1887

Journal of General Virology header logo

Volume 93, Issue 7

Non-canonical translation in RNA viruses Open Access

Abstract

Viral protein synthesis is completely dependent upon the translational machinery of the host cell. However, many RNA virus transcripts have marked structural differences from cellular mRNAs that preclude canonical translation initiation, such as the absence of a 5′ cap structure or the presence of highly structured 5′UTRs containing replication and/or packaging signals. Furthermore, whilst the great majority of cellular mRNAs are apparently monocistronic, RNA viruses must often express multiple proteins from their mRNAs. In addition, RNA viruses have very compact genomes and are under intense selective pressure to optimize usage of the available sequence space. Together, these features have driven the evolution of a plethora of non-canonical translational mechanisms in RNA viruses that help them to meet these challenges. Here, we review the mechanisms utilized by RNA viruses of eukaryotes, focusing on internal ribosome entry, leaky scanning, non-AUG initiation, ribosome shunting, reinitiation, ribosomal frameshifting and stop-codon readthrough. The review will highlight recently discovered examples of unusual translational strategies, besides revisiting some classical cases.

  • Published Online:
© 2012 SGM
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.042499-0
2012-07-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/7/1385.html?itemId=/content/journal/jgv/10.1099/vir.0.042499-0&mimeType=html&fmt=ahah

References

  1. Adams M. J., Antoniw J. F., Mullins J. G. 2001; Plant virus transmission by plasmodiophorid fungi is associated with distinctive transmembrane regions of virus-encoded proteins. Arch Virol 146:1139–1153 [View Article][PubMed]
     [Google Scholar]
  2. Agranovsky A. A., Koonin E. V., Boyko V. P., Maiss E., Frötschl R., Lunina N. A., Atabekov J. G. 1994; Beet yellows closterovirus: complete genome structure and identification of a leader papain-like thiol protease. Virology 198:311–324 [View Article][PubMed]
     [Google Scholar]
  3. Ahlquist P. 2006; Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4:371–382 [View Article][PubMed]
     [Google Scholar]
  4. Ahmadian G., Randhawa J. S., Easton A. J. 2000; Expression of the ORF-2 protein of the human respiratory syncytial virus M2 gene is initiated by a ribosomal termination-dependent reinitiation mechanism. EMBO J 19:2681–2689 [View Article][PubMed]
     [Google Scholar]
  5. Alam S. L., Wills N. M., Ingram J. A., Atkins J. F., Gesteland R. F. 1999; Structural studies of the RNA pseudoknot required for readthrough of the gag-termination codon of murine leukemia virus. J Mol Biol 288:837–852 [View Article][PubMed]
     [Google Scholar]
  6. Atkins J. F., Gesteland R. F. 2010 Recoding: Expansion of Decoding Rules Enriches Gene Expression Heidelberg: Springer; [CrossRef]
     [Google Scholar]
  7. Balvay L., Soto Rifo R., Ricci E. P., Decimo D., Ohlmann T. 2009; Structural and functional diversity of viral IRESes. Biochim Biophys Acta 1789:542–557[PubMed] [CrossRef]
     [Google Scholar]
  8. Barry J. K., Miller W. A. 2002; A −1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc Natl Acad Sci U S A 99:11133–11138 [View Article][PubMed]
     [Google Scholar]
  9. Beier H., Grimm M. 2001; Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res 29:4767–4782 [View Article][PubMed]
     [Google Scholar]
  10. Belsham G. J. 2005; Translation and replication of FMDV RNA. Curr Top Microbiol Immunol 288:43–70 [View Article][PubMed]
     [Google Scholar]
  11. Belsham G. J. 2009; Divergent picornavirus IRES elements. Virus Res 139:183–192 [View Article][PubMed]
     [Google Scholar]
  12. Bertram G., Innes S., Minella O., Richardson J., Stansfield I. 2001; Endless possibilities: translation termination and stop codon recognition. Microbiology 147:255–269[PubMed]
     [Google Scholar]
  13. Boeck R., Curran J., Matsuoka Y., Compans R., Kolakofsky D. 1992; The parainfluenza virus type 1 P/C gene uses a very efficient GUG codon to start its C′ protein. J Virol 66:1765–1768[PubMed]
     [Google Scholar]
  14. Bonetti B., Fu L., Moon J., Bedwell D. M. 1995; The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae . J Mol Biol 251:334–345 [View Article][PubMed]
     [Google Scholar]
  15. Boros Á., Pankovics P., Simmonds P., Reuter G. 2011; Novel positive-sense, single-stranded RNA (+ssRNA) virus with di-cistronic genome from intestinal content of freshwater carp (Cyprinus carpio). PLoS One 6:e29145 [View Article][PubMed]
     [Google Scholar]
  16. Brault V., van den Heuvel J. F., Verbeek M., Ziegler-Graff V., Reutenauer A., Herrbach E., Garaud J. C., Guilley H., Richards K., Jonard G. 1995; Aphid transmission of beet western yellows luteovirus requires the minor capsid read-through protein P74. EMBO J 14:650–659[PubMed]
     [Google Scholar]
  17. Brierley I., Gilbert R. J. C., Pennell S. 2010; Pseudoknot-dependent programmed −1 ribosomal frameshifting: structures, mechanisms and models. In Recoding: Expansion of Decoding Rules Enriches Gene Expression pp. 149–174 Edited by Atkins J. F., Gesteland R. F. Heidelberg: Springer; [View Article]
     [Google Scholar]
  18. Brown J. D., Ryan M. D. 2010; Ribosome “skipping”: “stop-carry on” or “StopGo” translation. In Recoding: Expansion of Decoding Rules Enriches Gene Expression pp. 101–121 Edited by Atkins J. F., Gesteland R. F. Heidelberg: Springer; [View Article]
     [Google Scholar]
  19. Brown C. M., Dinesh-Kumar S. P., Miller W. A. 1996; Local and distant sequences are required for efficient readthrough of the barley yellow dwarf virus PAV coat protein gene stop codon. J Virol 70:5884–5892[PubMed]
     [Google Scholar]
  20. Cao F., Tavis J. E. 2011; RNA elements directing translation of the duck hepatitis B virus polymerase via ribosomal shunting. J Virol 85:6343–6352 [View Article][PubMed]
     [Google Scholar]
  21. Castaño A., Ruiz L., Hernández C. 2009; Insights into the translational regulation of biologically active open reading frames of Pelargonium line pattern virus. Virology 386:417–426 [View Article][PubMed]
     [Google Scholar]
  22. Çevik B. 2001 Characterization of the RNA-dependent RNA polymerase gene of citrus tristeza closterovirus. PhD dissertation, University of Florida
  23. Chamond N., Locker N., Sargueil B. 2010; The different pathways of HIV genomic RNA translation. Biochem Soc Trans 38:1548–1552 [View Article][PubMed]
     [Google Scholar]
  24. Chaudhry Y., Nayak A., Bordeleau M. E., Tanaka J., Pelletier J., Belsham G. J., Roberts L. O., Goodfellow I. G. 2006; Caliciviruses differ in their functional requirements for eIF4F components. J Biol Chem 281:25315–25325 [View Article][PubMed]
     [Google Scholar]
  25. Chen W., Calvo P. A., Malide D., Gibbs J., Schubert U., Bacik I., Basta S., O’Neill R., Schickli J. other authors 2001; A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312 [View Article][PubMed]
     [Google Scholar]
  26. Choi I. R., Hall J. S., Henry M., Zhang L., Hein G. L., French R., Stenger D. C. 2001; Contributions of genetic drift and negative selection on the evolution of three strains of wheat streak mosaic tritimovirus. Arch Virol 146:619–628 [View Article][PubMed]
     [Google Scholar]
  27. Chung B. Y., Miller W. A., Atkins J. F., Firth A. E. 2008; An overlapping essential gene in the Potyviridae . Proc Natl Acad Sci U S A 105:5897–5902 [View Article][PubMed]
     [Google Scholar]
  28. Cimino P. A., Nicholson B. L., Wu B., Xu W., White K. A. 2011; Multifaceted regulation of translational readthrough by RNA replication elements in a tombusvirus. PLoS Pathog 7:e1002423 [View Article][PubMed]
     [Google Scholar]
  29. Clyde K., Harris E. 2006; RNA secondary structure in the coding region of dengue virus type 2 directs translation start codon selection and is required for viral replication. J Virol 80:2170–2182 [View Article][PubMed]
     [Google Scholar]
  30. Curran J., Kolakofsky D. 1988; Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA. EMBO J 7:245–251[PubMed]
     [Google Scholar]
  31. Daughenbaugh K. F., Wobus C. E., Hardy M. E. 2006; VPg of murine norovirus binds translation initiation factors in infected cells. Virol J 3:33 [View Article][PubMed]
     [Google Scholar]
  32. de Breyne S., Monney R. S., Curran J. 2004; Proteolytic processing and translation initiation: two independent mechanisms for the expression of the Sendai virus Y proteins. J Biol Chem 279:16571–16580 [View Article][PubMed]
     [Google Scholar]
  33. Dinesh-Kumar S. P., Miller W. A. 1993; Control of start codon choice on a plant viral RNA encoding overlapping genes. Plant Cell 5:679–692 [View Article][PubMed]
     [Google Scholar]
  34. Donnelly M. L., Luke G., Mehrotra A., Li X., Hughes L. E., Gani D., Ryan M. D. 2001; Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal ‘skip’. J Gen Virol 82:1013–1025[PubMed]
     [Google Scholar]
  35. Doronina V. A., Wu C., de Felipe P., Sachs M. S., Ryan M. D., Brown J. D. 2008; Site-specific release of nascent chains from ribosomes at a sense codon. Mol Cell Biol 28:4227–4239 [View Article][PubMed]
     [Google Scholar]
  36. Dreher T. W., Miller W. A. 2006; Translational control in positive strand RNA plant viruses. Virology 344:185–197 [View Article][PubMed]
     [Google Scholar]
  37. Dulude D., Berchiche Y. A., Gendron K., Brakier-Gingras L., Heveker N. 2006; Decreasing the frameshift efficiency translates into an equivalent reduction of the replication of the human immunodeficiency virus type 1. Virology 345:127–136 [View Article][PubMed]
     [Google Scholar]
  38. Edgil D., Harris E. 2006; End-to-end communication in the modulation of translation by mammalian RNA viruses. Virus Res 119:43–51 [View Article][PubMed]
     [Google Scholar]
  39. Ernst H., Shatkin A. J. 1985; Reovirus hemagglutinin mRNA codes for two polypeptides in overlapping reading frames. Proc Natl Acad Sci U S A 82:48–52 [View Article][PubMed]
     [Google Scholar]
  40. Firth A. E., Chung B. Y., Fleeton M. N., Atkins J. F. 2008; Discovery of frameshifting in alphavirus 6K resolves a 20-year enigma. Virol J 5:108 [View Article][PubMed]
     [Google Scholar]
  41. Firth A. E., Wills N. M., Gesteland R. F., Atkins J. F. 2011; Stimulation of stop codon readthrough: frequent presence of an extended 3′ RNA structural element. Nucleic Acids Res 39:6679–6691 [View Article][PubMed]
     [Google Scholar]
  42. Fuller F., Bhown A. S., Bishop D. H. 1983; Bunyavirus nucleoprotein, N, and a non-structural protein, NSs, are coded by overlapping reading frames in the S RNA. J Gen Virol 64:1705–1714 [View Article][PubMed]
     [Google Scholar]
  43. Fütterer J., Hohn T. 1991; Translation of a polycistronic mRNA in the presence of the cauliflower mosaic virus transactivator protein. EMBO J 10:3887–3896[PubMed]
     [Google Scholar]
  44. Fütterer J., Kiss-László Z., Hohn T. 1993; Nonlinear ribosome migration on cauliflower mosaic virus 35S RNA. Cell 73:789–802 [View Article][PubMed]
     [Google Scholar]
  45. Fütterer J., Potrykus I., Bao Y., Li L., Burns T. M., Hull R., Hohn T. 1996; Position-dependent ATT initiation during plant pararetrovirus rice tungro bacilliform virus translation. J Virol 70:2999–3010[PubMed]
     [Google Scholar]
  46. Fütterer J., Rothnie H. M., Hohn T., Potrykus I. 1997; Rice tungro bacilliform virus open reading frames II and III are translated from polycistronic pregenomic RNA by leaky scanning. J Virol 71:7984–7989[PubMed]
     [Google Scholar]
  47. Gibbs A. J., Keese P. K. 1995; In search of the origins of viral genes. In Molecular Basis of Virus Evolution pp. 76–90 Edited by Gibbs A. J., Calisher C. H., Garcia-Arenal F. Cambridge: Cambridge University Press; [View Article]
     [Google Scholar]
  48. Giedroc D. P., Cornish P. V. 2009; Frameshifting RNA pseudoknots: structure and mechanism. Virus Res 139:193–208 [View Article][PubMed]
     [Google Scholar]
  49. Goodman R. P., Freret T. S., Kula T., Geller A. M., Talkington M. W., Tang-Fernandez V., Suciu O., Demidenko A. A., Ghabrial S. A. other authors 2011; Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonasvirus species (family Totiviridae). J Virol 85:4258–4270 [View Article][PubMed]
     [Google Scholar]
  50. Gould P. S., Easton A. J. 2007; Coupled translation of the second open reading frame of M2 mRNA is sequence dependent and differs significantly within the subfamily Pneumovirinae . J Virol 81:8488–8496 [View Article][PubMed]
     [Google Scholar]
  51. Hemmings-Mieszczak M., Hohn T., Preiss T. 2000; Termination and peptide release at the upstream open reading frame are required for downstream translation on synthetic shunt-competent mRNA leaders. Mol Cell Biol 20:6212–6223 [View Article][PubMed]
     [Google Scholar]
  52. Herbert T. P., Brierley I., Brown T. D. 1996; Detection of the ORF3 polypeptide of feline calicivirus in infected cells and evidence for its expression from a single, functionally bicistronic, subgenomic mRNA. J Gen Virol 77:123–127 [View Article][PubMed]
     [Google Scholar]
  53. Horvath C. M., Williams M. A., Lamb R. A. 1990; Eukaryotic coupled translation of tandem cistrons: identification of the influenza B virus BM2 polypeptide. EMBO J 9:2639–2647[PubMed]
     [Google Scholar]
  54. Houck-Loomis B., Durney M. A., Salguero C., Shankar N., Nagle J. M., Goff S. P., D’Souza V. M. 2011; An equilibrium-dependent retroviral mRNA switch regulates translational recoding. Nature 480:561–564[PubMed]
     [Google Scholar]
  55. Ingolia N. T., Lareau L. F., Weissman J. S. 2011; Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:789–802 [View Article][PubMed]
     [Google Scholar]
  56. Ivanov I. P., Loughran G., Atkins J. F. 2008; uORFs with unusual translational start codons autoregulate expression of eukaryotic ornithine decarboxylase homologs. Proc Natl Acad Sci U S A 105:10079–10084 [View Article][PubMed]
     [Google Scholar]
  57. Jacks T., Varmus H. E. 1985; Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science 230:1237–1242 [View Article][PubMed]
     [Google Scholar]
  58. Jacks T., Madhani H. D., Masiarz F. R., Varmus H. E. 1988; Signals for ribosomal frameshifting in the Rous sarcoma virus gag–pol region. Cell 55:447–458 [View Article][PubMed]
     [Google Scholar]
  59. Jackson R. J., Hellen C. U., Pestova T. V. 2010; The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127 [View Article][PubMed]
     [Google Scholar]
  60. Jackson R. J., Hellen C. U., Pestova T. V. 2012; Termination and post-termination events in eukaryotic translation. Adv Protein Chem Struct Biol 86:45–93 [View Article][PubMed]
     [Google Scholar]
  61. Jang S. K., Kräusslich H. G., Nicklin M. J., Duke G. M., Palmenberg A. C., Wimmer E. 1988; A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol 62:2636–2643[PubMed]
     [Google Scholar]
  62. Jang C. J., Lo M. C., Jan E. 2009; Conserved element of the dicistrovirus IGR IRES that mimics an E-site tRNA/ribosome interaction mediates multiple functions. J Mol Biol 387:42–58 [View Article][PubMed]
     [Google Scholar]
  63. Kanyuka K. V., Vishnichenko V. K., Levay K. E., Kondrikov D. Y., Ryabov E. V., Zavriev S. K. 1992; Nucleotide sequence of shallot virus X RNA reveals a 5′-proximal cistron closely related to those of potexviruses and a unique arrangement of the 3′-proximal cistrons. J Gen Virol 73:2553–2560 [View Article][PubMed]
     [Google Scholar]
  64. Karasev A. V., Boyko V. P., Gowda S., Nikolaeva O. V., Hilf M. E., Koonin E. V., Niblett C. L., Cline K., Gumpf D. J. other authors 1995; Complete sequence of the citrus tristeza virus RNA genome. Virology 208:511–520 [View Article][PubMed]
     [Google Scholar]
  65. Kieft J. S. 2008; Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 33:274–283 [View Article][PubMed]
     [Google Scholar]
  66. Kim S. N., Choi J. H., Park M. W., Jeong S. J., Han K. S., Kim H. J. 2005; Identification of the +1 ribosomal frameshifting site of LRV1-4 by mutational analysis. Arch Pharm Res 28:956–962 [View Article][PubMed]
     [Google Scholar]
  67. Kneller E. L., Rakotondrafara A. M., Miller W. A. 2006; Cap-independent translation of plant viral RNAs. Virus Res 119:63–75 [View Article][PubMed]
     [Google Scholar]
  68. Kolakofsky D., Roux L., Garcin D., Ruigrok R. W. 2005; Paramyxovirus mRNA editing, the “rule of six” and error catastrophe: a hypothesis. J Gen Virol 86:1869–1877 [View Article][PubMed]
     [Google Scholar]
  69. Kong W. P., Roos R. P. 1991; Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyelitis virus. J Virol 65:3395–3399[PubMed]
     [Google Scholar]
  70. Kozak M. 1986; Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292 [View Article][PubMed]
     [Google Scholar]
  71. Kozak M. 1990; Downstream secondary structure facilitates recognition of initiator codons by eukaryotic ribosomes. Proc Natl Acad Sci U S A 87:8301–8305 [View Article][PubMed]
     [Google Scholar]
  72. Kozak M. 1991; A short leader sequence impairs the fidelity of initiation by eukaryotic ribosomes. Gene Expr 1:111–115[PubMed]
     [Google Scholar]
  73. Kozak M. 2002; Pushing the limits of the scanning mechanism for initiation of translation. Gene 299:1–34 [View Article][PubMed]
     [Google Scholar]
  74. Kozak M. 2004; How strong is the case for regulation of the initiation step of translation by elements at the 3′ end of eukaryotic mRNAs?. Gene 343:41–54 [View Article][PubMed]
     [Google Scholar]
  75. Kozak M. 2007; Lessons (not) learned from mistakes about translation. Gene 403:194–203 [View Article][PubMed]
     [Google Scholar]
  76. Laprevotte I., Hampe A., Sherr C. J., Galibert F. 1984; Nucleotide sequence of the gag gene and gag–pol junction of feline leukemia virus. J Virol 50:884–894[PubMed]
     [Google Scholar]
  77. Li W. Z., Qu F., Morris T. J. 1998; Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans . Virology 244:405–416 [View Article][PubMed]
     [Google Scholar]
  78. Li H., Havens W. M., Nibert M. L., Ghabrial S. A. 2011; RNA sequence determinants of a coupled termination-reinitiation strategy for downstream open reading frame translation in Helminthosporium victoriae virus 190S and other victoriviruses (family Totiviridae). J Virol 85:7343–7352 [View Article][PubMed]
     [Google Scholar]
  79. Loughran G., Firth A. E., Atkins J. F. 2011; Ribosomal frameshifting into an overlapping gene in the 2B-encoding region of the cardiovirus genome. Proc Natl Acad Sci U S A 108:E1111–E1119 [View Article][PubMed]
     [Google Scholar]
  80. Lukavsky P. J. 2009; Structure and function of HCV IRES domains. Virus Res 139:166–171 [View Article][PubMed]
     [Google Scholar]
  81. Luke G. A., de Felipe P., Lukashev A., Kallioinen S. E., Bruno E. A., Ryan M. D. 2008; Occurrence, function and evolutionary origins of ‘2A-like’ sequences in virus genomes. J Gen Virol 89:1036–1042 [View Article][PubMed]
     [Google Scholar]
  82. Luttermann C., Meyers G. 2007; A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA. J Biol Chem 282:7056–7065 [View Article][PubMed]
     [Google Scholar]
  83. Luttermann C., Meyers G. 2009; The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev 23:331–344 [View Article][PubMed]
     [Google Scholar]
  84. Martin R. R., Zhou J., Tzanetakis I. E. 2011; Blueberry latent virus: an amalgam of the Partitiviridae and Totiviridae . Virus Res 155:175–180 [View Article][PubMed]
     [Google Scholar]
  85. Matsuda D., Dreher T. W. 2006; Close spacing of AUG initiation codons confers dicistronic character on a eukaryotic mRNA. RNA 12:1338–1349 [View Article][PubMed]
     [Google Scholar]
  86. McCaughan K. K., Brown C. M., Dalphin M. E., Berry M. J., Tate W. P. 1995; Translational termination efficiency in mammals is influenced by the base following the stop codon. Proc Natl Acad Sci U S A 92:5431–5435 [View Article][PubMed]
     [Google Scholar]
  87. McCormick C. J., Salim O., Lambden P. R., Clarke I. N. 2008; Translation termination reinitiation between open reading frame 1 (ORF1) and ORF2 enables capsid expression in a bovine norovirus without the need for production of viral subgenomic RNA. J Virol 82:8917–8921 [View Article][PubMed]
     [Google Scholar]
  88. McFadden N., Bailey D., Carrara G., Benson A., Chaudhry Y., Shortland A., Heeney J., Yarovinsky F., Simmonds P. other authors 2011; Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 7:e1002413 [View Article][PubMed]
     [Google Scholar]
  89. Melian E. B., Hinzman E., Nagasaki T., Firth A. E., Wills N. M., Nouwens A. S., Blitvich B. J., Leung J., Funk A. other authors 2010; NS1′ of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J Virol 84:1641–1647 [View Article][PubMed]
     [Google Scholar]
  90. Meyers G. 2003; Translation of the minor capsid protein of a calicivirus is initiated by a novel termination-dependent reinitiation mechanism. J Biol Chem 278:34051–34060 [View Article][PubMed]
     [Google Scholar]
  91. Miller W. A., White K. A. 2006; Long-distance RNA–RNA interactions in plant virus gene expression and replication. Annu Rev Phytopathol 44:447–467 [View Article][PubMed]
     [Google Scholar]
  92. Miller W. A., Wang Z., Treder K. 2007; The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs. Biochem Soc Trans 35:1629–1633 [View Article][PubMed]
     [Google Scholar]
  93. Miyauchi K., Komano J., Myint L., Futahashi Y., Urano E., Matsuda Z., Chiba T., Miura H., Sugiura W., Yamamoto N. 2006; Rapid propagation of low-fitness drug-resistant mutants of human immunodeficiency virus type 1 by a streptococcal metabolite sparsomycin. Antivir Chem Chemother 17:167–174[PubMed] [CrossRef]
     [Google Scholar]
  94. Morozov S. Y., Solovyev A. G. 2003; Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol 84:1351–1366 [View Article][PubMed]
     [Google Scholar]
  95. Morris D. R., Geballe A. P. 2000; Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635–8642 [View Article][PubMed]
     [Google Scholar]
  96. Nakagawa S., Niimura Y., Gojobori T., Tanaka H., Miura K. 2008; Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes. Nucleic Acids Res 36:861–871 [View Article][PubMed]
     [Google Scholar]
  97. Namy O., Rousset J. P. 2010; Specification of standard amino acids by stop codons. In Recoding: Expansion of Decoding Rules Enriches Gene Expression pp. 79–100 Edited by Atkins J. F., Gesteland R. F. Heidelberg: Springer; [View Article]
     [Google Scholar]
  98. Namy O., Moran S. J., Stuart D. I., Gilbert R. J., Brierley I. 2006; A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 441:244–247 [View Article][PubMed]
     [Google Scholar]
  99. Napthine S., Lever R. A., Powell M. L., Jackson R. J., Brown T. D., Brierley I. 2009; Expression of the VP2 protein of murine norovirus by a translation termination–reinitiation strategy. PLoS One 4:e8390 [View Article][PubMed]
     [Google Scholar]
  100. Napthine S., Yek C., Powell M. L., Brown T. D., Brierley I. 2012; Characterization of the stop codon readthrough signal of Colorado tick fever virus segment 9 RNA. RNA 18:241–252 [View Article][PubMed]
     [Google Scholar]
  101. Nicholson B. L., White K. A. 2011; 3′ Cap-independent translation enhancers of positive-strand RNA plant viruses. Curr Opin Virol 1:373–380 [View Article][PubMed]
     [Google Scholar]
  102. Nitta T., Kuznetsov Y., McPherson A., Fan H. 2010; Murine leukemia virus glycosylated Gag (gPr80 gag ) facilitates interferon-sensitive virus release through lipid rafts. Proc Natl Acad Sci U S A 107:1190–1195 [View Article][PubMed]
     [Google Scholar]
  103. Ogle J. M., Brodersen D. E., Clemons W. M. Jr, Tarry M. J., Carter A. P., Ramakrishnan V. 2001; Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292:897–902 [View Article][PubMed]
     [Google Scholar]
  104. Olivier V., Blanchard P., Chaouch S., Lallemand P., Schurr F., Celle O., Dubois E., Tordo N., Thiéry R. other authors 2008; Molecular characterisation and phylogenetic analysis of chronic bee paralysis virus, a honey bee virus. Virus Res 132:59–68 [View Article][PubMed]
     [Google Scholar]
  105. Pelletier J., Sonenberg N. 1988; Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320–325 [View Article][PubMed]
     [Google Scholar]
  106. Plant E. P., Dinman J. D. 2005; Torsional restraint: a new twist on frameshifting pseudoknots. Nucleic Acids Res 33:1825–1833 [View Article][PubMed]
     [Google Scholar]
  107. Plant E. P., Rakauskaite R., Taylor D. R., Dinman J. D. 2010; Achieving a golden mean: mechanisms by which coronaviruses ensure synthesis of the correct stoichiometric ratios of viral proteins. J Virol 84:4330–4340 [View Article][PubMed]
     [Google Scholar]
  108. Polson A. G., Bass B. L., Casey J. L. 1996; RNA editing of hepatitis delta virus antigenome by dsRNA–adenosine deaminase. Nature 380:454–456 [View Article][PubMed]
     [Google Scholar]
  109. Pooggin M. M., Fütterer J., Skryabin K. G., Hohn T. 1999; A short open reading frame terminating in front of a stable hairpin is the conserved feature in pregenomic RNA leaders of plant pararetroviruses. J Gen Virol 80:2217–2228[PubMed]
     [Google Scholar]
  110. Pooggin M. M., Ryabova L. A., He X., Fütterer J., Hohn T. 2006; Mechanism of ribosome shunting in rice tungro bacilliform pararetrovirus. RNA 12:841–850 [View Article][PubMed]
     [Google Scholar]
  111. Powell M. L. 2010; Translational termination-reinitiation in RNA viruses. Biochem Soc Trans 38:1558–1564 [View Article][PubMed]
     [Google Scholar]
  112. Powell M. L., Leigh K. E., Pöyry T. A., Jackson R. J., Brown T. D., Brierley I. 2011; Further characterisation of the translational termination-reinitiation signal of the influenza B virus segment 7 RNA. PLoS One 6:e16822 [View Article][PubMed]
     [Google Scholar]
  113. Pöyry T. A., Kaminski A., Connell E. J., Fraser C. S., Jackson R. J. 2007; The mechanism of an exceptional case of reinitiation after translation of a long ORF reveals why such events do not generally occur in mammalian mRNA translation. Genes Dev 21:3149–3162 [View Article][PubMed]
     [Google Scholar]
  114. Prats A. C., De Billy G., Wang P., Darlix J. L. 1989; CUG initiation codon used for the synthesis of a cell surface antigen coded by the murine leukemia virus. J Mol Biol 205:363–372 [View Article][PubMed]
     [Google Scholar]
  115. Qu X., Wen J. D., Lancaster L., Noller H. F., Bustamante C., Tinoco I. Jr 2011; The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 475:118–121 [View Article][PubMed]
     [Google Scholar]
  116. Racine T., Duncan R. 2010; Facilitated leaky scanning and atypical ribosome shunting direct downstream translation initiation on the tricistronic S1 mRNA of avian reovirus. Nucleic Acids Res 38:7260–7272 [View Article][PubMed]
     [Google Scholar]
  117. Rancurel C., Khosravi M., Dunker A. K., Romero P. R., Karlin D. 2009; Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 83:10719–10736 [View Article][PubMed]
     [Google Scholar]
  118. Raoult D., Forterre P. 2008; Redefining viruses: lessons from mimivirus. Nat Rev Microbiol 6:315–319 [View Article][PubMed]
     [Google Scholar]
  119. Ren Q., Wang Q. S., Firth A. E., Chan M. M., Gouw J. W., Guarna M. M., Foster L. J., Atkins J. F., Jan E. 2012; Alternative reading frame selection mediated by a tRNA-like domain of an internal ribosome entry site. Proc Natl Acad Sci U S A 109:E630–E639[PubMed] [CrossRef]
     [Google Scholar]
  120. Sanchez A., Trappier S. G., Mahy B. W., Peters C. J., Nichol S. T. 1996; The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. Proc Natl Acad Sci U S A 93:3602–3607 [View Article][PubMed]
     [Google Scholar]
  121. Scheets K., Blinkova O., Melcher U., Palmer M. W., Wiley G. B., Ding T., Roe B. A. 2011; Detection of members of the Tombusviridae in the Tallgrass Prairie Preserve, Osage County, Oklahoma, USA. Virus Res 160:256–263 [View Article][PubMed]
     [Google Scholar]
  122. Schepetilnikov M., Schott G., Katsarou K., Thiébeauld O., Keller M., Ryabova L. A. 2009; Molecular dissection of the prototype foamy virus (PFV) RNA 5′-UTR identifies essential elements of a ribosomal shunt. Nucleic Acids Res 37:5838–5847 [View Article][PubMed]
     [Google Scholar]
  123. Schepetilnikov M., Kobayashi K., Geldreich A., Caranta C., Robaglia C., Keller M., Ryabova L. A. 2011; Viral factor TAV recruits TOR/S6K1 signalling to activate reinitiation after long ORF translation. EMBO J 30:1343–1356 [View Article][PubMed]
     [Google Scholar]
  124. Schmidt-Puchta W., Dominguez D., Lewetag D., Hohn T. 1997; Plant ribosome shunting in vitro . Nucleic Acids Res 25:2854–2860 [View Article][PubMed]
     [Google Scholar]
  125. Scholthof H. B., Gowda S., Wu F. C., Shepherd R. J. 1992; The full-length transcript of a caulimovirus is a polycistronic mRNA whose genes are trans activated by the product of gene VI. J Virol 66:3131–3139[PubMed]
     [Google Scholar]
  126. Sedman S. A., Gelembiuk G. W., Mertz J. E. 1990; Translation initiation at a downstream AUG occurs with increased efficiency when the upstream AUG is located very close to the 5′ cap. J Virol 64:453–457[PubMed]
     [Google Scholar]
  127. Skabkin M. A., Skabkina O. V., Dhote V., Komar A. A., Hellen C. U., Pestova T. V. 2010; Activities of Ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev 24:1787–1801 [View Article][PubMed]
     [Google Scholar]
  128. Skuzeski J. M., Nichols L. M., Gesteland R. F., Atkins J. F. 1991; The signal for a leaky UAG stop codon in several plant viruses includes the two downstream codons. J Mol Biol 218:365–373 [View Article][PubMed]
     [Google Scholar]
  129. Su H. M., Tai J. H. 1996; Genomic organization and sequence conservation in type I Trichomonas vaginalis viruses. Virology 222:470–473 [View Article][PubMed]
     [Google Scholar]
  130. Taylor J. M. 2006; Hepatitis delta virus. Virology 344:71–76 [View Article][PubMed]
     [Google Scholar]
  131. Thiébeauld O., Pooggin M. M., Ryabova L. A. 2007; Alternative translation strategies in plant viruses. Plant Viruses 1:1–20
     [Google Scholar]
  132. Tork S., Hatin I., Rousset J. P., Fabret C. 2004; The major 5′ determinant in stop codon read-through involves two adjacent adenines. Nucleic Acids Res 32:415–421 [View Article][PubMed]
     [Google Scholar]
  133. Touriol C., Bornes S., Bonnal S., Audigier S., Prats H., Prats A. C., Vagner S. 2003; Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol Cell 95:169–178 [View Article][PubMed]
     [Google Scholar]
  134. Turina M., Desvoyes B., Scholthof K. B. 2000; A gene cluster encoded by panicum mosaic virus is associated with virus movement. Virology 266:120–128 [View Article][PubMed]
     [Google Scholar]
  135. van der Wilk F., Dullemans A. M., Verbeek M., Van den Heuvel J. F. 1997; Nucleotide sequence and genomic organization of Acyrthosiphon pisum virus. Virology 238:353–362 [View Article][PubMed]
     [Google Scholar]
  136. van Eyll O., Michiels T. 2002; Non-AUG-initiated internal translation of the L* protein of Theiler’s virus and importance of this protein for viral persistence. J Virol 76:10665–10673 [View Article][PubMed]
     [Google Scholar]
  137. Vassilaki N., Mavromara P. 2009; The HCV ARFP/F/core+1 protein: production and functional analysis of an unconventional viral product. IUBMB Life 61:739–752 [View Article][PubMed]
     [Google Scholar]
  138. Vera-Otarola J., Solis L., Soto-Rifo R., Ricci E. P., Pino K., Tischler N. D., Ohlmann T., Darlix J. L., López-Lastra M. 2012; The Andes hantavirus NSs protein is expressed from the viral small mRNA by a leaky scanning mechanism. J Virol 86:2176–2187 [View Article][PubMed]
     [Google Scholar]
  139. Verchot J., Angell S. M., Baulcombe D. C. 1998; In vivo translation of the triple gene block of potato virus X requires two subgenomic mRNAs. J Virol 72:8316–8320[PubMed]
     [Google Scholar]
  140. Volchkova V. A., Dolnik O., Martinez M. J., Reynard O., Volchkov V. E. 2011; Genomic RNA editing and its impact on Ebola virus adaptation during serial passages in cell culture and infection of guinea pigs. J Infect Dis 204:Suppl 3S941–S946 [View Article][PubMed]
     [Google Scholar]
  141. Walewski J. L., Keller T. R., Stump D. D., Branch A. D. 2001; Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7:710–721 [View Article][PubMed]
     [Google Scholar]
  142. Walsh D., Mohr I. 2011; Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 9:860–875 [View Article][PubMed]
     [Google Scholar]
  143. Wei T., Zhang C., Hong J., Xiong R., Kasschau K. D., Zhou X., Carrington J. C., Wang A. 2010; Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6:e1000962 [View Article][PubMed]
     [Google Scholar]
  144. Wells S. E., Hillner P. E., Vale R. D., Sachs A. B. 1998; Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2:135–140 [View Article][PubMed]
     [Google Scholar]
  145. Wen R. H., Hajimorad M. R. 2010; Mutational analysis of the putative pipo of soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400:1–7 [View Article][PubMed]
     [Google Scholar]
  146. Williams M. A., Lamb R. A. 1989; Effect of mutations and deletions in a bicistronic mRNA on the synthesis of influenza B virus NB and NA glycoproteins. J Virol 63:28–35[PubMed]
     [Google Scholar]
  147. Wilson J. E., Pestova T. V., Hellen C. U., Sarnow P. 2000; Initiation of protein synthesis from the A site of the ribosome. Cell 102:511–520 [View Article][PubMed]
     [Google Scholar]
  148. Wise H. M., Foeglein A., Sun J., Dalton R. M., Patel S., Howard W., Anderson E. C., Barclay W. S., Digard P. 2009; A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 83:8021–8031 [View Article][PubMed]
     [Google Scholar]
  149. Woo P. C., Lau S. K., Choi G. K., Huang Y., Teng J. L., Tsoi H. W., Tse H., Yeung M. L., Chan K. H. other authors 2012; Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. J Virol 86:2797–2808 [View Article][PubMed]
     [Google Scholar]
  150. Wulff B. E., Nishikura K. 2010; Substitutional A-to-I RNA editing. Wiley Interdiscip Rev RNA 1:90–101[PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.042499-0
Loading
Non-canonical translation in RNA viruses
J. Gen. Virol. 93, 1385 (2012); https://doi.org/10.1099/vir.0.042499-0
/content/journal/jgv/10.1099/vir.0.042499-0
/content/journal/jgv/10.1099/vir.0.042499-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error